Life before impact in the Chicxulub area: unique marine ichnological signatures preserved in crater suevite

To fully assess the resilience and recovery of life in response to the Cretaceous–Paleogene (K-Pg) boundary mass extinction ~ 66 million years ago, it is paramount to understand biodiversity prior to the Chicxulub impact event. The peak ring of the Chicxulub impact structure offshore the Yucatán Peninsula (México) was recently drilled and extracted a ~ 100 m thick impact-generated, melt-bearing, polymict breccia (crater suevite), which preserved carbonate clasts with common biogenic structures. We pieced this information to reproduce for the first time the macrobenthic tracemaker community and marine paleoenvironment prior to a large impact event at the crater area by combining paleoichnology with micropaleontology. A variable macrobenthic tracemaker community was present prior to the impact (Cenomanian–Maastrichtian), which included soft bodied organisms such as annelids, crustaceans and bivalves, mainly colonizing softgrounds in marine oxygenated, nutrient rich, conditions. Trace fossil assemblage from these upper Cretaceous core lithologies, with dominant Planolites and frequent Chondrites, corresponds well with that in the overlying post-impact Paleogene sediments. This reveals that the K-Pg impact event had no significant effects (i.e., extinction) on the composition of the macroinvertebrate tracemaker community in the Chicxulub region.

, and Lowery et al. 7 . For detailed location of drilling sites see Gulick et al. 21 . www.nature.com/scientificreports/ The location of the Chicxulub impact was a carbonate ramp with an average water depth of 600 m 20 , wherein the carbonate ramp deepened from ~ 100 m water depth in the south-southwest to approximately 2 km in the north-northeast 20,34 . The depositional environment during the early Paleocene at Site M0077 corresponded to the upper and/or middle bathyal zone at ~ 600-700 m depth 7 . Sedimentary target clasts from the studied suevite sequence mainly correspond to sediment derived from coastal and shallow-water environments that prevailed throughout much of the paleo-Gulf of Mexico 35 . The sediment clasts of the suevite were initially emplaced by processes initiated by the impact 5,28 , and subsequently deposited in the crater by a powerful ocean resurge 28 , which most probably entered the Chicxulub crater through a N-NE gap in the outer rim 5,12,20,21,28 (Fig. 1).
Previous work on the Cretaceous part of the Yucatán's target stratigraphy, based on outcrop studies in both México 24 and in adjacent northern Belize 36,37 , indicated that shallow-water carbonate facies of the target Yucatán Group show similarities with the limestone clasts in the suevite (see Ormö et al. 28 , for a recent analysis). The sedimentary, (upper) target carbonates could be further subdivided into two main groups for more information of their provenance, the 'upper target I' and the 'upper target II' carbonates 28 . The 'upper target I' carbonates likely derive from the upper part of the Yucatán Group, which is equivalent to the informal Barton Creek Formation in Belize and the Campur Formation of Guatemala, with a Campanian-Maastrichtian age 36 , and 'upper target II' likely come from the lower Yucatan Group, which is equivalent to the informal Yalbac formation of Belize and of the Coban Formation of Guatemala 36 . Recent analysis of lithological features and carbonate rock textures of the Barton and Yalbac formation supported that interpretation that target carbonates derived from these formations 95 . Therefore, the trace-fossil bearing carbonate clasts from Hole M0077A likely originated from the upper part of the Yucatán Group target. In the Tabasco-Chiapas-Campeche region, the impact-generated limestone megabreccia of the Guayal and Bochil K-Pg sections also contains foraminifera suggesting a Maastrichtian age 39 .
In the recovered Yax-1 core from the annular trough of the Chicxulub impact structure (Fig. 1), six suevitic units were differentiated in a ∼ 100 m thick impactite sequence, revealing a mixture of late Campanian to early Maastrichtian nannofossil assemblage in the uppermost three suevite units 40,41 . The mixed nature of reworked Campanian to Maastrichtian microfossils, together with lithic fragments and impact derived materials in the suevite of units 2 and 1 in Yax-1 core is similar to the K-Pg boundary "cocktail" deposits in the Gulf of Mexico 42 . The Late Cretaceous biostratigraphic age range found for the studied carbonate clasts within the IODP-ICDP Exp. 364 M0077A core (see detailed biostratigraphic data from the studied clasts in the Micropaleontology and biostratigraphy section) agrees, in part, with observations of planktic foraminifera within the matrix throughout the entire suevite sequence from the same drill core 12 and from carbonate clasts within Unit 2A 21 . In addition, rare and moderately to poorly preserved nannofossils were reported in the upper part of the M0077A graded suevite between 619.27 and 677.22 mbsf that indicate a Late Cretaceous stratigraphic range 21 .

Results
Biogenic sedimentary and bioerosion structures in the suevite.. Suevite from Hole M0077A, referred to as Unit 2 21 , is characterized by a clastic matrix and is dominated by vitric and microcrystalline impact melt rock clasts and fragments from the sedimentary cover and the crystalline basement, the latter displaying varying degrees of shock metamorphism 12,21 . Clasts from target sedimentary lithologies in the suevite mainly include carbonates, both as primary, fossil-bearing clasts, and as altered carbonate clasts, and rare siltstone and chert clasts 12,28 . Isolated Cretaceous planktic foraminifera are present throughout the entire 100 m thick suevite sequence, although the non-graded suevite unit and the bedded suevite unit show more abundant planktic foraminifera in the matrix compared to the graded suevite unit 12 .
Biogenic sedimentary structures are quite common and relatively diverse within the carbonate clasts of the suevite in the M0077A drill core. The ichnological analysis of the entire suevite at Site M0077 reveals biogenic sedimentary structures in core segments from Unit 2B (55R_003-11 cm to 83R_001-75 cm), in particular from core segments between 61_R_002 to 82_R_002 (see Supplementary information and Fig. 2B,C), between core depths ∼679-711 mbsf. Core segments belonging to Unit 2A (40R_1-109.4 cm to 55R_3-11 cm) contain small clasts (in general < 1 cm), and those from Unit 2C (83R_1-75 cm to 87R_2-90 cm), show mainly recrystallized carbonate clasts, wherein biogenic structures can rarely be recognized.
The biogenic sedimentary structures are mainly preserved in light brown carbonate clasts, usually between 1 and 5 cm in size and locally up to 20 cm, observed in several core segments of the lower part of the graded suevite unit and the upper part of the non-graded suevite unit (Figs. 2, 3; Kaskes et al. 12 ). The most abundant trace fossil is Planolites, registered in the 86% of the studied clasts, which appears in almost all the studied core segments as circular to subcircular, cylindrical, tubular forms of a variable size (diameter 2-4 mm, length 5-20 mm; Figs. 2C, 3A-G, S1). The record of other ichnotaxa is frequent as in the case of Chondrites (36% of the clasts), or sporadic for ?Asterosoma (14% of the clasts) and Teichichnus (T. zigzag) (5% of the clasts) (Fig. S1). ?Asterosoma are observed as bulbous forms, in light-gray and brown carbonate clasts usually together with Planolites (Figs. 2C, 3B). Chondrites are mainly observed in brown carbonate clasts (Figs. 2C, 3D-E,F), usually on a mottled background, as short tubes or circular to elliptical spots, 1-2 mm in diameter. One specimen of Teichichnus zigzag is observed in a light brown carbonate clast (Figs. 2C, 3G), appearing as a wall-like spreite (e.g., laminated biogenic structure) structure with a zig-zag vertical section, 2-3 cm in length and 0.5 to 1 cm in diameter. Biodeformational structures as those showing undifferentiated outlines and the absence of a defined geometry producing a mottled fabric are observed in several clasts (45%). In some carbonate clasts (Figs. 2C, 3C-F), the mottled background is crosscut by discrete Chondrites and Planolites. A bioerosion structure appearing as a single cylindrical form, less than 5 mm long, observed in a light brown clast (label 11 in Fig. 2C

Micropaleontology and biostratigraphy.
A selection of the suevite carbonate clasts containing ichnological features was investigated for micropaleontological content to assess their depositional environment and geological age (Supplementary Table 1). The majority of the studied clasts are wackestones and packstones with a micritic matrix and a variable fossil content with grains < 2 mm, including shell fragments, calcispheres, calcareous nannoplankton and planktic and benthic foraminifera of variable preservation (Fig. 4)

Discussion
The pre-impact macrobenthic tracemaker community in the Chicxulub area. The ichnological record from the Chicxulub peak-ring suevite provides unique insights on the macrobenthic tracemaker community living at 'ground zero' during the Late Cretaceous, especially given the scarcity of other ichnological information from the Yucatán area (see Supplementary information). Scarce ichnological data was documented www.nature.com/scientificreports/ far (more than 1.000 km) from the Chicxulub impact crater area, as from the Navarro-Taylor Sequence, the last unit deposited in the Gulf of Mexico prior to the Chicxulub impact event 46 . Campanian Taylor sandstones from the Serbin field (southern Texas) commonly contain Ophiomorpha and irregular, burrowed tops; Planolites typically overlie the tops of these sandstones. In addition, Cruziana ichnofacies was reported suggesting that the depositional environment was shallow marine and close to the shoreline 26 . In northern Louisiana, Shellhouse 27 presented a description of a cored succession including contacts between the K-Pg boundary unit and the underlying chalk of the Navarro Group NT supersequence 47 . The cored succession can be subdivided into three main units, indicating the presence of abundant Thalassinoides and Chondrites in the lower unit, Thalassinoides and Helminthopsis in the middle unit, and rare Helminthopsis in the upper unit. In Northeastern Mexico, an abundant and diverse Late Cretaceous ichnofauna, with Chondrites, Ophiomorpha, Planolites and Zoophycos was documented 48 .
The ichnological data can help to assess paleoenvironmental, paleoecological and depositional conditions in the Yucatán area. Moreover, such data also serve as a reference in comparisons with the life forms inhabiting the crater after the drastic paleoenvironmental changes caused by the Chicxulub impact. The presence of a mottled background in several clasts (Fig. 3C-F) reveals the activity of tracemakers at the sediment water interface or just below the sea floor, in softground, causing the complete destruction of primary structures by the shallowest burrowing organisms 49 . This observation points to general paleoenvironmental conditions on the sea bed favorable for diverse life forms. Thus, oxic bottom and pore waters in the upper part of the bioturbated zone, and available organic matter, allowed for the development of a shallow tier macrobenthic community. Planolites (Fig. 3A-G) is a facies-crossing form, featuring actively filled burrows, interpreted as a grazing trace reflecting a combination of locomotion and feeding (pascichnion) most likely produced by soft bodied invertebrates (i.e., wormlike animals) in diverse environments [50][51][52] . Planolites is usually interpreted as a shallow tier trace fossil, and its dominance or exclusiveness can be related to environmental parameters favorable for the tracemakers (i.e., oxic and nutrient rich conditions), supporting the interpretation of the origin of the mottled background. Asterosoma (Fig. 3B) is commonly considered as a feeding trace (fodinichnion) produced by polychaete and other worms or suspension-feeding animals, such as certain crustaceans 53 . This trace is frequently registered in a wide range of marine environments, from paralic to deep-marine settings, commonly associated with well-oxygenated conditions 53 . Chondrites (Fig. 3D-F) shows a wide range of morphologies, and many organisms are proposed producers, such as annelids (e.g., polychaetes), siphunculans, or bivalves 53 . Chondrites may be considered a facies-crossing form, registered in a variety of facies and environments. However, it is usually interpreted as a good indicator of dysoxic settings, where the dissolved oxygen in bottom and pore waters is between 0.2 and 1 ml/l 53 , frequently observed in deep-marine environments. The behavior of the tracemaker is variable, possibly resulting from subsurface deposit-feeding behavior, suspension-feeding, detritus-feeding on the sea floor, or it could even be interpreted as a chemosymbiotic organism; the trace is produced preferentially in fine-grained softgrounds and locally in relatively cohesive substrates 53 . Teichichnus zigzag (Fig. 3G) is associated with the activity-mainly suspension and deposit feeding-of worm-like animals (e.g., annelids), but also arthropods (e.g., crustaceans) and bivalves, preferentially in silty and muddy sand softgrounds 53 . Teichichnus zigzag is usually observed in siliciclastic, marginal-marine to shallow-marine settings. Teichichnus zigzag can be interpreted as an equilibrium trace due to changes in sedimentation and erosion as occur in the upper shoreface, tidal flat, delta plain, etc. 53 . The presence of a bioerosion structure, probable Gastrochaenolites (Fig. 3H), is related to consolidated or cemented sedimentary materials in proximal areas. These settings such as firmgrounds or hardgrounds, are colonized by boring bivalves 54,55 . The late cretaceous Yucatán sea. Ichnological data reveal the presence of a diverse macrobenthic tracemaker community in the Yucatán area during the Cenomanian to the Maastrichtian, including soft bodied organisms such as annelids and shelly animals including crustaceans and bivalves. These organisms mainly colonized softgrounds at the sediment water interface or just below the sea floor, as a feeding activity. Bioerosion structures in firmground-hardgrounds were likely formed by bivalves. This diverse tracemaker community points towards a variety of habitats and paleoenvironmental conditions ranging from coastal to shelfal and more pelagic environments. In this context, distance to shore, suggested to be 800 km away 5 based on a paleogeographic reconstruction of shorelines 56,57 , and bathymetry are important parameters to be considered. Most of the observed biogenic structures, including the probable Gastrochaenolites, were formed in a wide range of paleoenvironments, but mainly in shelfal settings. However, Chondrites is usually registered in deeper environments than the rest of the recognized ichnotaxa, which supports variability in the paleowater depth related to the initial formation of the sedimentary clasts before they brecciated, transported and became part of the suevite sequence. Thus, deep-water carbonate facies were probably incorporated into the M0077A suevite sequence, as evidenced with large quantities of planktic foraminifera and nannofossils in the lower part of the suevite.
The Chicxulub impact event and its effect on macrobenthic biota. The registered softground trace fossil assemblage consisting of dominant Planolites, frequent Chondrites, and very rare ?Asterosoma and Teichichnus (T. zigzag), is quite similar (mainly consisting of Planolites and Chondrites and rare Palaeophycus) to that observed in the first phase of diversification (diversification I) 14 after the initial recovery that occurred within years to decades after the impact event, as recorded in the Transitional Interval in the M0077A core ( Fig. 2) 5,7,11,13 . Particularly, the most frequent assemblage (29% of the clasts) consisting of Planolites and Chondrites overprinting a mottled background registered in the Upper Cretaceous clasts is similar to the assemblage observed at the early Paleocene sediments 14 (Fig. S1). Moreover, ichnotaxa from the Upper Cretaceous clasts show similar dimensions than those from the early Paleocene. However, abundance of traces (as BI) is higher at the Upper Cretaceous clasts 14 (Fig.S1) www.nature.com/scientificreports/ from the early Paleocene sediments, are more diverse, abundant and consisting of larger traces, that the trace fossil assemblage corresponding to the initial recovery just after the K-Pg event 14 (Fig. S1). In this initial recovery phase, trace fossil assemblage is low abundant (BI ~ 1), and mainly consists of smaller Planolites (< 4 mm size), and very scarce Chondrites (< 1 mm size) 14 (Fig. S1). Even though the ichnological information in this study is fragmentary as it is derived from target clasts, some interpretations with respect to the ecological consequences of the impact event on the macrobenthic tracemaker community can be made. The similarity in trace fossil assemblage and in size of traces in Upper Cretaceous and early Paleocene sediments in the crater area agrees with the absence of significant effects (i.e., extinction) of the Chicxulub impact event on the global marine macrobenthic tracemaker community, and the rapid recovery of the macrobenthic tracemaker community, as previously observed in distal K-Pg boundary sections such as in Spain and Denmark 4,49,50,52,[58][59][60][61][62] . Pre-impact macrobenthic tracemaker community during Upper Cretaceous, dominated by the shallow and middle tiers, is similar, but more abundant, that the post-impact community registered during the early Paleocene. In between, the initial recovery phase occurred within several years after the K-Pg boundary impact, is characterized by a less diverse and scarcer trace fossil assemblage 14 . This comparatively minor disruption and the rapid return to the pre-extinction macrobenthic tracemaker community of the impact site 6 could be related to the existence of less affected habitats outside the crater and then migration of these biota into the crater when favourable conditions were re-established. This finding implies rapid recolonization of the impact site 7,11 by the macrobenthic tracemaker community. Trace fossils of this community do not appear at the base of the Transitional Unit but rather within the upper ~ 30 cm of it, which likely represents a few years after impact 5,9,13 . This suggestion is in line with other data which suggest that the crater seafloor may not have yet been habitable for a brief period after the impact 7 .

Materials and methods
The entire 98.3 m thick suevite unit (617.33 mbsf, 40R-1-109.4 cm to 715.6 mbsf, 84R-3-78 cm) in core M0077A was preliminary studied. This unit was subdivided into Units 2A, 2B and 2C 21 based on sedimentary features and matrix composition. Then, this interval was divided into a bedded suevite, graded suevite and non-graded suevite unit that are a distinct in petrography, geochemistry, and sedimentology 12 . Unit 2B, from 664.52 mbsf (55R-3-11 cm) to 712.84 mbsf (83R-1-75 cm) contains abundant clasts in which biogenic structures and/or fossils were observed due to a generally larger clast size than in the Unit 2A above (Kaskes et al.) 12 ; this was the selected interval studied in detail. The suevite at Site M0077 was studied for ichnological features through a detailed visual examination of high-resolution digital images of the 83 mm wide archive half cores, including Core overview, Line Scan, and X-ray computed tomography (CT, CTA, and CTD) images, using a digital image methodology [63][64][65] (see Supplementary information). This processing enhanced the structures of interest in the images allowing better recognition of variable types of biogenic structures, as biogenic sedimentary structures and bioerosion structures, and the ichnotaxonomical classification of discrete trace fossils [66][67][68] (see Supplementary information). In addition, biostratigraphic analyses were performed on ten polished 30 µm thin sections of the investigated carbonate clasts by means of a micropaleontological assessment focusing on the taxonomy of planktic and benthic foraminifera, and nannofossil analysis.

Data availability
All data generated or analysed during this study are included in this published article [and its supplementary information files]. The datasets generated and/or analysed during the current study are not publicly available due to size restrictions, but are available from the corresponding author on reasonable request.